RESEARCH ARTICLE

A mixed method multi-country assessment of

barriers to implementing pediatric inpatient

care guidelines

Kirkby D. TickellID1,2, Dorothy I. Mangale2, Stephanie N. Tornberg-BelangerID

1,2,

Celine Bourdon3, Johnstone Thitiri4, Molline Timbwa4, Jenala Njirammadzi5,

Wieger Voskuijl5,6, Mohammod J. Chisti7, Tahmeed Ahmed7, Abu S. M. S. B. Shahid7,

Abdoulaye H. Diallo8,9, Issaka Ouedrago10, Al Fazal KhanID7, Ali F. Saleem11,

Fehmina Arif12, Zaubina Kazi11, Ezekiel MupereID13, John Mukisa13, Priya Sukhtankar4,

James A. BerkleyID4, Judd L. Walson1,2,14,15, Donna M. Denno2,15,16*, on behalf of the

Childhood Acute Illness and Nutrition Network¶

1 Department of Epidemiology, University of Washington, Seattle, Washington, United States of America,

2 Department of Global Health, University of Washington, Seattle, Washington, United States of America,

3 Program in Translational Medicine, The Hospital for Sick Children, Toronto, Ontario, Canada, 4 KEMRI-

Wellcome Trust Research Programe, Kilifi, Kenya, 5 Department of Paediatrics, College of Medicine,

University of Malawi, Blantyre, Malawi, 6 Global Child Health Group, Emma Children’s Hospital, Amsterdam

University Medical Centre, Amsterdam, the Netherlands, 7 Centre for Nutrition & Food Security (CNFS),

icddr, b, Dhaka, Bangladesh, 8 Department of Public Health, Centre MURAZ Research Institute, Ministry of

Health, Bobo-Dioulasso, Burkina Faso, 9 Department of Public Health, University of Ouagadougou,

Ouagadougou, Burkina Faso, 10 Department of Paediatrics, Banfora Regional Referral Hospital, Banfora,

Burkina Faso, 11 Department of Paediatrics and Child Health, Aga Khan University, Karachi, Pakistan,

12 Department of Paediatrics, Civil Hospital Karachi, Karachi, Pakistan, 13 Department of Paediatrics and

Child Health, College of Health Sciences, Makerere University, Kampala, Uganda, 14 Department of

Medicine, University of Washington, Seattle, Washington, United States of America, 15 Department of

Pediatrics, University of Washington, Seattle, Washington, United States of America, 16 Department of

Health Services, University of Washington, Seattle, Washington, United States of America

¶ Current membership of the Childhood Acute Illness & Nutrition (CHAIN) Network, Nairobi, Kenya, can be

found in S1 Appendix.

* ddenno@uw.edu

Abstract

Introduction

Accelerating progress in reducing child deaths is needed in order to achieve the Sustainable

Development Goal child mortality target. This will require a focus on vulnerable children–

including young children, those who are undernourished or with acute illnesses requiring hos-

pitalization. Improving adherence to inpatient guidelines may be an important strategy to

reduce child mortality, including among the most vulnerable. The aim of our assessment of

nine sub-Saharan African and South Asian hospitals was to determine adherence to pediatric

inpatient care recommendations, in addition to capacity for and barriers to implementation of

guideline-adherent care prior to commencing the Childhood Acute Illness and Nutrition

(CHAIN) Cohort study. The CHAIN Cohort study aims to identify modifiable risk factors for

poor inpatient and post discharge outcomes above and beyond implementation of guidelines.

Methods

Hospital infrastructure, staffing, durable equipment, and consumable supplies such as medi-

cines and laboratory reagents, were evaluated through observation and key informant

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OPEN ACCESS

Citation: Tickell KD, Mangale DI, Tornberg-

Belanger SN, Bourdon C, Thitiri J, Timbwa M, et al.

(2019) A mixed method multi-country assessment

of barriers to implementing pediatric inpatient care

guidelines. PLoS ONE 14(3): e0212395. https://doi.

org/10.1371/journal.pone.0212395

Editor: Ricardo Q. Gurgel, Federal University of

Sergipe, BRAZIL

Received: August 6, 2018

Accepted: January 27, 2019

Published: March 25, 2019

Copyright: © 2019 Tickell et al. This is an open

access article distributed under the terms of the

Creative Commons Attribution License, which

permits unrestricted use, distribution, and

reproduction in any medium, provided the original

author and source are credited.

Data Availability Statement: Deidentified datasets

are available from Dryad.org (https://doi.org/10.

5061/dryad.898m083).

Funding: This study was funded by the Bill and

Melinda Gates Foundation (OPP1131320). The

funders had no role in study design, data collection

and analysis, decision to publish, or preparation of

the manuscript.

Competing interests: The authors have declared

that no competing interests exist.

interviews. Inpatient medical records of 2–23 month old children were assessed for adher-

ence to national and international guidelines. The records of children with severe acute mal-

nutrition (SAM) were oversampled to reflect the CHAIN study population. Seven core

adherence indicators were examined: oximetry and oxygen therapy, fluids, anemia diagno-

sis and transfusion, antibiotics, malaria testing and antimalarials, nutritional assessment

and management, and HIV testing.

Results

All sites had facilities and equipment necessary to implement care consistent with World

Health Organization and national guidelines. However, stockouts of essential medicines

and laboratory reagents were reported to be common at some sites, even though they were

mostly present during the assessment visits. Doctor and nurse to patient ratios varied

widely. We reviewed the notes of 261 children with admission diagnoses of sepsis (17),

malaria (47), pneumonia (70), diarrhea (106), and SAM (119); 115 had multiple diagnoses.

Adherence to oxygen therapy, antimalarial, and malnutrition refeeding guidelines was

>75%. Appropriate antimicrobials were prescribed for 75% of antibiotic-indicative condi-

tions. However, 20/23 (87%) diarrhea and 20/27 (74%) malaria cases without a documented

indication were prescribed antibiotics. Only 23/122 (19%) with hemoglobin levels meeting

anemia criteria had recorded anemia diagnoses. HIV test results were infrequently docu-

mented even at hospitals with universal screening policies (66/173, 38%). Informants at all

sites attributed inconsistent guideline implementation to inadequate staffing.

Conclusion

Assessed hospitals had the infrastructure and equipment to implement guideline-consistent

care. While fluids, appropriate antimalarials and antibiotics, and malnutrition refeeding

adherence was comparable to published estimates from low- and high-resource settings,

there were inconsistencies in implementation of some other recommendations. Stockouts

of essential therapeutics and laboratory reagents were a noted barrier, but facility staff per-

ceived inadequate human resources as the primary constraint to consistent guideline

implementation.

Introduction

Global child mortality rates remain unacceptably high at 39 deaths per 1000 live births, despite

reductions over the past decades.[1] The vast majority of the more than five million under-5

deaths per annum occur in low-resource settings. To achieve the Sustainable Development

Goals child health target, accelerated progress is required which will necessitate focusing on

children at highest risk of death.[2] Standardized case management of acutely ill children

requiring hospitalization, based on World Health Organization (WHO) guidelines, has been

shown to reduce inpatient mortality, and many avoidable child deaths can be attributed to a

failure to administer recommended care.[3–7] However, hospitals implementing these guide-

lines still report high inpatient and post-discharge case fatality rates.[3,8–10]

The objective of the Childhood Acute Illness & Nutrition (CHAIN) Network is to build the

evidence base for improving outcomes of children most vulnerable to poor outcomes. These

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vulnerabilities include young age, undernutrition, and acute illness warranting hospitalization.

By recruiting a cohort of 2–23 month-old children at hospital admission and following them

six months post-discharge, the CHAIN Network aims to identify modifiable causes of inpa-

tient and post-discharge mortality beyond a failure to correctly implement existing guidelines.

The aim of the evaluation described in this paper was to determine clinical capacity, adherence

to pediatric inpatient care standards, and capacity for and barriers to implementation of guide-

line-adherent care at each site prior to the cohort study initiation. The nine Network sites

include: Dhaka and Matlab Hospitals (Bangladesh), the Civil Hospital Karachi (Pakistan),

Kilifi County Hospital (Kenya), Mbagathi District Hospital (Kenya), Migori Country Referral

Hospital (Kenya), Mulago Hospital (Uganda), Queen Elizabeth Central Hospital (Malawi),

and Banfora Regional Referral Hospital (Burkina Faso). This paper describes these sites, clini-

cal care delivered prior to beginning cohort recruitment, and the barriers to guideline imple-

mentation experienced by the Network hospitals.

Methods

We conducted a mixed method assessment of the nine CHAIN Network sites. Key health indi-

cators (fertility, under-five mortality, malaria incidence, and HIV, child wasting and stunting

prevalences) for the population served by each facility were extracted from publicly available

sources in order to provide a context for the sites. Our assessment framework and standard-

ized data collection tools (Table A in S1 File) were developed based on published quality of

care appraisals and WHO quality assessment references.[11–18] At least two assessment team

members (DD, DM, KT, PS, CB) visited each hospital between May 2016 and October 2017,

and collected information across five domains (listed below) through direct observation, clini-

cal notes review, and semi-structured interviews with key informants including pharmacists,

laboratory managers, hospital administrators, doctors, clinical officers, nurses, and research

staff. The interviews lasted approximately 30 minutes and were conducted by pairs of assess-

ment team members. No key informants refused participation. Salient concepts were recorded

in real time by an assessment team member on semi-structured standardized forms. Although

no formal thematic identification process was undertaken, paraphrased quotes and ideas were

used to form and triangulate key findings. Observations of equipment, medicines, and facilities

and abstractions of the clinical notes were also documented on standardized forms. All team

members were trained on use of data report forms prior to conducting the assessment.

Hospitals were expected to have a full complement of essential equipment and medicines,

and be able to provide a panel of basic laboratory tests as outlined below. No a priori cut-offs

for acceptable adherence to guidelines or clinical staffing were set, as we are unaware of any

validated norms that apply across the diversity of settings studied. However, results were com-

pared to other published literature from high- and low-resource settings (Table B in S1 File).

[12,18–27] The CHAIN Cohort study received ethical approval from Oxford University, Uni-

versity of Washington, and all Network sites. The funder had no role in the study or manu-

script development.

Hospital infrastructure & characteristics

Annual patient volumes, bed capacity, financing sources, participation in pre-service health

worker education, blood bank, medical waste disposal and equipment sterilization facilities,

and reliability of electricity and water supplies were assessed through key informant interviews

and administrative reports. Radiology services were characterized by access to bedside or cen-

tralized ultrasound scanning and 24-hour x-rays, based on clinician interviews. Clinical labo-

ratory staffing, external certification, availability of routine chemistries (electrolytes and

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creatinine), hematology (complete blood count), and microbiology (blood, cerebrospinal fluid,

stool, urine, wound cultures) were catalogued during direct observation of laboratories and

interviews with laboratory managers who were also asked about the frequency of reagent

stockouts.

A high dependency score, consisting of nine characteristics assessed by direct observation,

designed to capture high dependency or intensive care capacity (Table C in S1 File), was calcu-

lated at the facility level to reflect the highest capacity available to children at each institution.

The high dependency score, and the essential equipment score (below), were also tabulated for

all inpatient or pre-admission units which deliver substantial management, heuristically

defined by capacity to provide injectable antibiotics, to children aged 2–23 months (i.e.,

CHAIN Cohort eligible).

Essential medicines

The availability of potentially life-saving therapeutics, abstracted from the WHO Essential

Medicines List and guideline-recommended nutritional products (ready-to-use therapeutic

food (RUTF), ready-to-use supplementary food, milk formula-100 (F-100), and milk formula-

75 (F-75))[28–30] was assessed through observation and key informant interviews with staff

responsible for stock management. Informants were also asked if each item was subject to

occasional or frequent stockouts. Therapeutics considered exchangeable within guidelines

were condensed into a single-item category (e.g., normal saline and Ringer’s Lactate) and vali-

dated locally-made alternatives were accepted (e.g., milk suji formulations instead of F-75 and

F-100 in Bangladesh).

Essential equipment

An essential equipment inventory was adapted from published surveys and categorized into

those used to identify acute illness and malnutrition, treat acute illness and malnutrition, and

resuscitate children in cardiorespiratory decompensation.[12,13] Each item’s presence and

functionality was assessed through observation and clinical staff interviews.

Clinical care staffing

Pediatric care staff numbers were drawn from administrative data provided during interviews

with senior physicians, charge nurses/matrons, or hospital administrators. Cadre per 1,000

pediatric admissions, and per 100 beds available to CHAIN participants (e.g., excluding neona-

tal units), were calculated in order to provide comparable figures across facilities of different

sizes.

Clinical management

Inpatient notes of recently discharged or deceased children aged 2–23 months admitted for

acute illness were provided for our review by the sites. The CHAIN Cohort purposefully over-

samples children with severe acute malnutrition (SAM). To ensure SAM management was

adequately represented, therefore, approximately half of notes reviewed per hospital had a

SAM diagnosis. Key indicators of guideline adherence were extracted from the first 48 hours

of admission and grouped into seven core areas: 1) pulse oximetry and oxygen, 2) fluids, 3)

anemia diagnosis and transfusion, 4) antibiotics, 5) malaria diagnosis and antimalarials, 6)

nutritional assessment, SAM management, and young infant breastfeeding support, and 7)

HIV testing.

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Clinical practices were compared to WHO guidelines.[31,32] However, consistency with

institutional or national recommendations was also considered guideline adherent (Table B in

S1 File). Summary statistics, including estimating the proportion of children receiving adher-

ent care, were calculated using Stata 14.2 (StataCorps, College Station, Tx). Finally, interviews

with clinical staff were conducted to ascertain which discrepancies represented poor or collo-

quial documentation versus deviations from guideline recommended care.

Results

Hospital infrastructure and characteristics

Population and hospital characteristics: The CHAIN sites serve diverse populations across

sub-Saharan Africa and South Asia with varied disease epidemiology (Table 1). Patient vol-

umes also varied from 2,000 to 15,000 annual pediatric admissions per site, and hospitals had

one to ten pediatric or neonatal wards. Seven hospitals had separate SAM units (Table 2).

Financing: All CHAIN sites receive funding from their respective health ministries, but five

had additional sources. Matlab and Dhaka Hospitals receive support from bilateral donors.

QECH Pediatric Department partners with a charity that provides funds to stock a pediatric

pharmacy and supplement nursing staffing. At Civil Hospital, alumni and other local charities

have financed numerous initiatives, including building and staffing a pediatric intensive care

unit. The KEMRI-Wellcome Trust Research Programme supports Kilifi Hospital, including

Table 1. Population and disease epidemiology characteristics.

Hospital Name

Region/Province

Country

Site

Dhaka

Dhaka

Bangladesh

Matlab

Chittagong

Bangladesh

Civil

Sindh

Pakistan

Kilifi

Coast

Kenya

Mbagathi

Nairobi

Kenya

Migori

Nyanzaa

Kenya

Mulago

Kampala

Uganda

QECH

Southern

Malawi

Banfora

Cascades

Burkina Faso

Global

Country indicators

GDP/capita (2016) $1,359 $1,359 $1,444 $1,455 $1,455 $1,455 $580 $300 $627 $10,151

GDP/cap. rank (from lowest) 36th 36th 39th 40th 40th 40th 13th 2nd 14th —

U5MR (2017) 38 38 81 49 49 49 55 64 89 43

MDG4 achieved Yes Yes No No No No Yes Yes No No

Province indicators

Urban/Rural Urban Rural Urban Rural Urban Rural Urban Urban Rural —

Total fertility rateb 2.3 2.5 3.9 5.1 2.7 5.3 3.3 4.6 6.0 2.5

U5MRb 54 50 93 57 72 82 47 73 170 43

Malaria incidenceb,c 0 0d 0.0–0.1 50–100 0.0–0.1 200–300 200–300 10–50 >300 94f

HIV prevalence, 15-49Yb <0.1% <0.1% <0.1% 5%e 6%e 14%e 7% 15% 0.8% 1%

Wasting prevalence, <5Yb 12% 16% 14% 5% 3% 4% 4% 4% 12% 8%

Stunting prevalence, <5Yb 34% 38% 35% 31% 17% 26% 14% 37% 38% 24%

aNyanza Province is no longer an administrative region, but demographic health and surveillance data are still aggregated at this level.bBased on most recently available Demographic Health Survey data, therefore years vary.cIncidence is per 1000 population. Highly malaria endemic is defined as >1 case per 1000 population.dMalaria is endemic to eastern regions of Chittagong Division, but not Matlab.eKenyan HIV estimates listed are at the county rather than provincial level.fAmong at risk populations.

Abbreviations: Cap.: capita, GDP: gross domestic product, MDG4: Millennium Development Goal 4—Reduce the U5MR by two-thirds between 1990 and 2015, QECH:

Queen Elizabeth Central Hospital, U5MR: under-five mortality rate (deaths per 1000 live births), Y: year-olds.

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financing a high dependency unit, pediatric medicines, and salaries of researchers who also

serve as clinical consultants.

Patient fees: Seven sites provide free care to children under five. Mbagathi and Migori Hos-

pitals charge a subsidized daily inpatient fee of approximately $3.70 and $5.00, respectively,

with added charges for investigations and medications. At all sites, families are asked to pro-

cure medicines and supplies from other sources during stockouts.

Table 2. Hospital characteristics.

Hospitals

Dhaka

Bangladesh

Matlab

Bangladesh

Civil Pakistan Kilifi

Kenya

Mbagathi

Kenya

Migori

Kenya

Mulago

Uganda

QECH

Malawi

Banfora

Burkina Faso

Administration

Management IRO IRO MOH MOH MOH MOH MOH MOH MOH

University hospital — — Dow — — — Makerere Malawi Bobo-

Dioulasso

Teaching hospitala Yes Yes Yes Yes Yes Yes Yes Yes Yes

Patient volumes

Ages considered

pediatric

<5Y <5Y <13Y <13Y 1M – 13Y 1M – 13Y <18Y <14Y <15Y

Pediatric

admissions/year

4,600 2,500 7,500 4,000 2,000 2,000 15,000 12,500 4,000

Pediatric & neonatal

wards

4 3 5 2 1 1 5 10 4

Fees for pediatric

careb

None None None None Daily fee

+ incurred costs

Daily fee

+ incurred costs

None None None

Hospital

Infrastructure

Medical waste

disposal

Onsite

incinerator

Onsite

incinerator

Onsite

incinerator

Onsite

incinerator

Onsite incinerator Onsite incinerator Onsite

incinerator

Onsite

incinerator

Onsite

incinerator

Equipment

sterilization

Autoclave Autoclave Autoclave Autoclave Autoclave Autoclave Autoclave Chlorination Autoclave

Water supply

reliabilityc

100% 100% 95% 90% 90% 50% 100% 90% 90%

Electricity reliabilityc 100% 100% 30% 100% 90% 95% 90% 90% 95%

X-ray radiography 24/7 Wk days 8–5 24/7 24/7 Wk days 8–5 24/7 24/7 24/7 24/7

Ultrasound scanner In radiology In radiology In radiology Bedside No In radiology In radiology Bedside In radiology

Blood bank No No On-site On-site Off-site On-site On-site On-site On-site

Clinical Laboratory

Specimens per day 500 35 5000 120 250 300 500–650 500 150

In-hours staffing 60 6 150 1 5–8 10 26 14 3

Out-of-hours

staffing

1 1 10 1 1 1 0 1 3

External certification Yes No No Yes No No No No No

Routine testing

servicesd

Yes Yes Yes Yes Yese Yese Yes Yes Yes

Bactec blood culture Yes No Yes Yes No No Yes No No

HDC score 9/9 3/9 8/9 7/9 5/9 4/9 8/9 7/9 5/9

aDefined as including any clinician, nurse or nutritionist pre-service clinical clerkships.bIncurred costs include for medications and diagnostics.cExpressed as % of time reliably supplied according to key informants.dDefined as capacity to perform basic biochemistries (urea, creatinine and standard electrolytes), complete blood count, and cultures on urine, cerebrospinal fluid,

blood, wound, and stool specimens.eMbagathi and Migori had the full complement of clinical laboratory services assessed except the capacity to perform cultures on stool specimens.

Abbreviations: HDC: high dependency care, IRO: international research organization, M: month-olds, Wk: week, Y: year-olds.

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Clinical labs and radiology: All clinical laboratories have the infrastructure to provide basic

services, however, reagent stockouts intermittently disrupted services at Mulago, Mbagathi,

Migori, and Queen Elizabeth Central Hospitals. Sites unaffected by stockouts procured

reagents outside of governmental systems, except for Civil Hospital. Clinical laboratories at

two hospitals were externally certified. Ultrasonography was available at eight sites, while basic

radiography was present at all sites, either on pediatric units or in radiology departments, with

seven sites providing service on a 24-hour basis.

HDU/ICU: High dependency care scores range from 3–9 out of a maximum possible score

of 9 (Table C in S1 File). All sites had a high dependency care area on a ward or a self-con-

tained unit, devoted to the care of severe acute illness. All of these areas and units were at mini-

mum close to a nursing station and with access to oxygen. QECH and Kilifi and Mulago

Hospitals had dedicated high dependency units. Civil Hospital had a pediatric intensive care

unit and Dhaka Hospital had a combined adult and pediatric intensive care unit managed by a

pediatric intensivist.

Essential medicines

Essential medicines were largely available during assessment visits, but frequent stockouts

were reported (Table 3). F-75, F-100, and ReSoMal substitutes were prepared at Banfora, Mba-

gathi, and Kilifi Hospitals during stockouts, while the Migori Hospital nutrition team sought

products from other counties.

Some therapeutics were deliberately not stocked. Dhaka and Matlab Hospitals did not

maintain anti-retrovirals because patients with suspected or confirmed HIV infection are

referred to government facilities. Similarly, Banfora Hospital refers tuberculosis cases to a

regional center and does not stock anti-tuberculosis medications. Milk suji formulations are

used instead of F-75 and F-100 at Dhaka and Matlab Hospitals. Dhaka Hospital prepared

nutrient dense therapeutic foods in lieu of RUTF, which has not yet been approved for use in

Bangladesh, however, Matlab Hospital does not prepare these products. In Karachi, a high

density diet is used in place of RUTF.

Essential equipment

All hospitals had the range of essential equipment (Table 4) necessary for implementing guide-

line-based care at the time of their visit. Many sites had additional supplies (i.e., intubation

kits, cardio-respiratory monitors, continuous positive airway pressure, and infusion pumps)

allowing for enhanced care. Hospital composite scores were higher than individual wards’

scores (Table D in S1), due in large part to wards catering to specific conditions (e.g., nutri-

tional rehabilitation units do not require chest drains) or equipment sharing between wards.

Clinical care staffing

Pediatric human resources varied between hospitals (Table 5), but clinical and administrative

staff at all sites reported overextended human resources to be the most prominent barrier to

quality care. Doctors per 1,000 pediatric admissions ranged from 1.3–11.3, and were lower in

African hospitals, where task shifting to clinical officers was common. Consultant-level physi-

cians were more available at the urban sites, with the exception of Kilifi Hospital. QECH had

fewer consultants per admission than the other urban centers, but key informants reported

that senior doctor staffing levels are better than at other Malawian hospitals. Senior clinicians

at all the African sites reported that the rotation of junior doctors and clinical officers exacer-

bate low staff levels by creating a constant need for training and reinforcement of best clinical

practices.

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Nurse staffing levels were between 1.8–19.1 per 1,000 pediatric admissions. Key informants

at all sites reported that inadequate nurse staffing levels limit care such as anthropometric

screening, nutritional counselling and breast-feeding support. Nutritionists or dieticians were

employed at all sites excluding Banfora and Matlab Hospitals, and nursing assistants and lay

health workers were variably utilized.

All sites participated in health worker undergraduate or diploma training programs, and

the African sites’ senior clinicians and nurses noted that students are an important supplement

to human resource capacity, albeit inconsistent due to fluctuating trainee schedules.

Clinical management

Institutional or national adaptations of WHO guidelines were available as wall charts or in

handbooks on the ward at each site. The clinical notes of 261 children were reviewed (22–38

per site). Multiple diagnoses were noted in 115 cases. Cumulatively, there were seven shock, 17

Table 3. Essential medicines availability. Green—always in stock, yellow—occasional stockouts, red—frequent stockouts, black—never stocked.

Essential Medications Dhaka

Bangladesh

Matlab

Bangladesh

Civil Pakistan Kilifi

Kenya

Mbagathi

Kenya

Migori

Kenya

Mulago

Uganda

QECH

Malawi

Banfora

Burkina Faso

Antibiotics

Ampicillin/Benzyl penicillinGentamicinCeftriaxone

FlucloxacillinMacrolide

Ciprofloxacin1st line antiretrovirals

1st line antituberculosis drugs

Oral antimalariala

Injectable antimalariala

Emergency Medicines

AdrenalineAtropine

Intravenous or rectal short acting anti-convulsantsIntravenous or oral phenobarbitol or phenytoin

Intravenous fluids

Isotonic fluidsDextrose 5% or 10%Dextrose (�25%)

Oral rehydration solution (ORS)

Standard ORSReSoMal

Nutritional Therapeutics

Milk formula 75 (F-75b)Milk formula 100 (F-100b)

Ready-to-use therapeutic foodReady-to-use supplementary food

aOral: artemisinin-based combination therapies, Injectable: artensunate, artemether, quinine.bMilk suji equivalent used in Dhaka and Matlab hospitals

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sepsis, 47 malaria, 70 pneumonia, 106 diarrhea, and 119 SAM diagnoses. The median age at

admission was nine months (interquartile range (IQR): 6–15). Twenty-nine (11%) children

died during hospitalization, the median time from admission to death was three days (IQR

2–8). Excluding inpatient deaths, median length of stay was four days (IQR: 2–7).

Pulse oximetry and oxygen. Pulse oximetry was documented for 53/70 (76%) of children

with pneumonia diagnosed at admission. Hypoxia (oxygen saturation <90% in room air)[29]

was noted for 8/53 (12%) children with pneumonia diagnoses Oxygen orders were noted for

three-quarters of these children (6/8). Another 11 children with pneumonia diagnoses were

noted to be on oxygen, but had saturations above 90% or no recorded oxygen saturations, dur-

ing their admission examination.

Table 4. Availability of equipment for assessment, treatment and resuscitation. Black = functioning equipment not available, Green = equipment available and

functioning.

Equipment Dhaka

Bangladesh

Matlab

Bangladesh

Civil Pakistan Kilifi

Kenya

Mbagathi

Kenya

Migori

Kenya

Mulago

Uganda

QECH

Malawi

Banfora

Burkina Faso

Pulse oximeter

Cardio-respiratory monitor

Sphygmomanometer

Pediatric cuff

Point of care glucose strips

Torch/light source

Otoscope

Length board

Scales basin

Scales standing

Mid-upper arm circumference tapes

Suction equipment

Oxygen

Oxygen flow meter

Nebulizer/spacer with face mask & inhaler

Chest tubes

Pediatric cannulas (24 or 22 gauge)

Pediatric burette

Intraosseous set

Needles & syringes

Intravenous giving sets

Nasogastric tubes (gauges 8–10)

Infusion pump

Anti-epileptics on ward

Antibiotics on ward

Resuscitation table

Airways

Intubation set

Infant-size bag-valve mask

Child-size bag-valve mask

Adrenaline

Atropine

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Fluids. Intravenous fluid boluses are indicated for intravascular volume expansion in chil-

dren with severe dehydration or shock using isotonic fluids at 20 ml/kg (repeated as needed),

or for managing hypoglycemia with 10% dextrose at 5 ml/kg.[29] Twenty-seven children

(10%) had documented prescriptions of fluid boluses. Blood glucose levels were rarely

recorded, though among those noted as having received boluses, 17/27 (63%) appeared to be

for the prevention or management of hypoglycemia, suggested by the use of 10% dextrose

water solution at a median volume of 4.5 ml/kg (IQR: 3.0–4.9). The remaining 10 bolus vol-

umes were consistent with volume expansion (median volume of 34.4 ml/kg (IQR: 30–60)).

Nine of these 10 boluses were isotonic fluids, the other was dextrose saline. Dehydration status

was poorly documented, but 9/10 (90%) of the children who received volume expansion

boluses had documented potential indications (9 diarrhea, 3 shock, 1 sepsis).

Intravenous or oral rehydration was noted for 96/106 (91%) children with diarrhea, and

oral rehydration solution (ORS) was prescribed for 86/106 (81%). All 23 children with diarrhea

and SAM co-diagnoses were correctly prescribed ReSoMal or standard ORS according to local

guidelines.

Table 5. Pediatric care staffing at each hospital.

Cadre Dhaka

Bangladesh

Matlab

Bangladesh

Civil

Pakistan

Kilifi

Kenya

Mbagathi

Kenya

Migori

Kenya

Mulago

Uganda

QECH

Malawi

Banfora

Burkina Faso

N (per 1,000 pediatric admissions)

Doctors

Consultantsa 18 (3.9) 1 (0.4) 20 (2.7) 4 (1.0) 3 (1.5) 0 18 (1.3) 5 (0.4) 2 (0.5)

Pediatric post-graduate trainees 5 (1.1) 0 18 (2.4) 4 (1.0) 1 (1.5) 0 60 (4.0) 11 (0.9) 0

Medical officers 29 (6.3) 10 (4.0) 5 (0.7) 0 5 (2.5) 2 (0.7) 4 (0.3) 0 3 (0.8)

Interns 0 0 9 (1.1) 8 (2.0) 1 (0.5) 5 (1.7) 28 (1.8) 11 (0.9) 0

Total 52 (11.3) 11 (4.4) 52 (6.9) 16 (4.0) 10 (6.0) 7 (2.4) 110 (7.3) 27 (2.2) 5 (1.3)

Mid-level Providersb

Fully-licensed 0 0 0 3 (0.8) 2 (1.0) 3 (1.0) 1 (0.1) 0 0

Interns 0 0 0 7 (1.8) 5 (2.5) 0 0 0 0

Total 0 0 0 10 (1.8) 7 (3.5) 3 (1.0) 1 (0.1) 0 0

Nurses 88 (19.1) 17 (6.8) 42 (5.6) 32 (4.3) 12 (6.0) 7 (2.3) 85 (5.7) 34 (2.7) 44 (11.0)

Nursing assistants 8 (1.7) 0 9 (0.6) 0 0 0 9 (0.6) 15 (1.2) 0

Lay health workers 47 (10.2) 16 (6.4) 1 (0.1) 22 (5.5) 3 (1.5) 0 0 3 (0.2) 0

Nutritionistsc 5 (1.1) 0 1 (0.1) 3 (0.8) 2 (1.0) 3 (0.0) 3 (0.2) 1 (0.1) 0

Per 100 bedse

Doctorsc 78.8 11.2 30.1 27.6 21.7 26.9 36.5 15.5 3.5

Mid-level providersb 0 0 0 17.2 15.2 11.5 0.3 0 0

Nursesd 133.3 17.3 24.3 55.2 26.1 26.9 27.6 19.5 12.3

Nursing assistants 12.1 0 5.2 0 0 0 2.9 8.6 0

Lay health workers 71.2 16.3 0.6 37.9 6.5 0 0 1.7 0

Nutritionistsc 7.6 0 0.6 5.2 4.3 11.5 1.0 0.6 0

aClinical full time equivalent (i.e., time allocated to research not included). Remaining cadres are full time clinical staff.bClinical officers in Africa.c Typical beds-per-doctor on service during day-time hours were: Dhaka 4.3, Matlab 8.0, Civil 5.7, Kilifi 9.7, Mbagathi 11.5, Migori 6.5, Mulago 9.6, QECH 7.3, Banfora

22.0, with night-time ratios of: Dhaka 39.0, Matlab 28.0, Civil 14.0, Kilifi 58.0, Mbagathi 46.0, Migori 26.0, Mulago 44.0, QECH 58.0, Banfora 67.0.dTypical beds-per nurse during day-time hours were: Dhaka 9.8, Matlab 7.0, Civil 5.7, Kilifi 9.7, Mbagathi 23.0, Migori 26.0, Mulago 16.2, QECH 5.8, Banfora 16.8, with

night-time ratios of: Dhaka 13.0, Matlab 14.0, Civil 6.7, Kilifi 9.7, Mbagathi 23.0, Migori 26.0, Mulago 34.2, QECH 19.3, Banfora 16.8.eAvailable to CHAIN patients (e.g., not including neonatal units).

https://doi.org/10.1371/journal.pone.0212395.t005

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Anemia diagnosis and transfusion. Hemoglobin concentrations were recorded in the

notes of 167 (64%) children and in 96/148 (65%) of those admitted to sites with high malaria

endemicity (African sites excluding Mbagathi Hospital in Nairobi). The WHO anemia diag-

nostic criteria (hemoglobin <11g/dl)[29,31] was met by 122/167 children, but only 23 (19%)

had an explicit diagnosis in their clinical notes. Among children with severe anemia (hemoglo-

bin<7g/dl), 10/28 (36%) had a corresponding diagnosis.

The WHO recommends blood transfusion for hemoglobin <4.0 g/dl, hemoglobin�4.0

and<6.0 g/dl with clinical signs of shock, dehydration, respiratory acidosis, impaired con-

sciousness, heart failure, or severe hyperparasitemia. Persistent shock unresponsive to appro-

priate intravenous fluid resuscitation is also indication for transfusion regardless of

hemoglobin status.[29,31] For the purposes of this assessment, transfusions were considered

indicated if there was documentation of shock or of a hemoglobin concentration <6g/dl.

Thirty-five children had transfusions ordered, 31 (89%) of whom had a documented hemoglo-

bin result, and 23/35 (66%) had a documented potential indication including 18/35 (51%) with

hemoglobin <6 g/dl and an additional five with shock diagnoses. Clinicians at three sites

reported challenges obtaining blood products (Kilifi, Dhaka, Matlab Hospitals), however,

informants at all but Kilifi Hospital indicated that this rarely affected care.

Antibiotic management. Antibiotics were prescribed to 168/170 (99%) children with a

documented indication at admission. Overall, 128/170 (75%) of these regimens were adherent

to guidelines. Adherent regimens were prescribed to 78/106 (74%) with SAM, 60/70 (86%)

with pneumonia, 16/17 (94%) with sepsis, and 8/12 (67%) with meningitis.

Antibiotics are not recommended for malaria or diarrhea without dysentery or suspected

cholera unless there is a comorbidity necessitating antibiotics. Among 108 children with a

diagnosis of diarrhea, 105 (97%) were prescribed antibiotics. However, 67 had SAM, 17 had

another comorbidity warranting antimicrobials, and one had dysentery. Twenty (90%) of the

23 children with diarrhea and no documented indication for antibiotics were prescribed

antibiotics.

Thirty-nine (83%) of 47 children with malaria diagnoses were prescribed antibiotics,

including 20/27 (74%) without documented comorbid indications for antibiotics. Thirteen of

these 20 (65%) had a recorded positive malaria test, one had a negative malaria test noted, and

six did not have a documented malaria test.

Malaria diagnosis and antimalarials. At highly malaria endemic sites, 49/68 (72%) chil-

dren with febrile temperature measurements had malaria test results recorded, predominantly

by parasite smears. Thirty-three children without documented fever also had recorded malarial

test results. Thirty-seven of the 82 (45%) test results were noted to be positive, and all but one

child with confirmed malaria were prescribed antimalarials. One child with a negative result

and 10 without documented test results were prescribed an antimalarial. All antimalarials pre-

scribed were guideline-adherent.

Nutritional assessment, SAM management, and breastfeeding support for young

infants. Six sites screened all pediatric inpatients for SAM, while three did so based on clini-

cal suspicion only. Assessment was by Gomez classification at one site, weight-for-height Z

score the remainder, and six sites additionally employed mid-upper arm circumference

(MUAC). Anthropometric status was noted in 136 (52%) patient notes, though at two sites

with systematic screening and electronic capture systems, the values were not obviously visible,

and were therefore missed by the assessment team. The WHO recommends F-75 at refeeding

rates of 130 mls/kg/day for SAM (100mls/kg/day for kwashiorkor) acute phase management.

[29] Ninety-three (78%) of the 119 patients diagnosed with SAM had recorded feeding rates.

The median initial feeding rate was 128 ml/kg/day (IQR: 107–133).

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For young infants (age <6 months) with SAM, eight hospitals used dilute F-100 to supple-

ment breastmilk, and one never supplemented breastmilk (QECH). All sites offered breast-

feeding support, irrespective of nutritional status. Six hospitals provided relactation support

for mothers of young infants who had ceased breastfeeding. Five hospitals did not have materi-

als or infrastructure (e.g., play room or toys) to provide play therapy recommended for psy-

chosocial stimulation for inpatient children with SAM.[30,33]

The management of moderate acute malnutrition (MAM) varied across sites. Migori Hos-

pital managed these children according to SAM refeeding recommendations. At Dhaka and

Matlab Hospitals, all pediatric inpatients received specific milk-based or lactose-free feeds,

including those with MAM. QECH and Kilifi, Mbagathi, and Mulago Hospitals provided a

two-week supply of corn-soy blend at discharge, while in Banfora Hospital caregivers received

nutritional education without food supplementation. No specific MAM interventions were

delivered at Civil Hospital.

HIV testing. The African sites aimed for universal HIV screening of pediatric admissions,

but only 65/173 (38%) children admitted to these hospitals had HIV test results documented

in their notes. Interviewees attributed this deficit to concealment of results (e.g., locally specific

codes or log-books outside of patient notes). Three sites reported interruptions in universal

screening and follow-up care due to test kit stockouts, inadequate staffing, or siloed HIV pro-

grams. The Asian sites tested or referred for testing based on clinical suspicion only, and no

test results were identified in our notes review.

Discussion

All CHAIN Network sites had the infrastructure, equipment, and access to guidelines neces-

sary to provide care consistent with current recommendations. Several sites had enhanced

care capacity, such as a high dependency unit. Given that all sites’ facilities and equipment

enable their ability to meet minimum care standards as defined by WHO pediatric inpatient

care guidelines, capacity above this expectation is a welcome addition to the Network. The

additional resources were largely supported by charitable donations, philanthropic support, or

research infrastructure that play a critical role at five sites. These hospitals were also least

affected by stockouts of laboratory reagents and medicines, as these commodities could be sup-

plemented by research or charitable partnerships (QECH and Civil and Kilifi Hospitals) or

they relied exclusively on non-governmental procurement channels (Dhaka and Matlab Hos-

pitals). The other four sites reported laboratory reagents and medicines to be common and a

barrier to quality patient care.

The clinical notes review demonstrated that adherence to recommended care was inconsis-

tent. Perfect guideline adherence may be undesirable, as some deviations reflect appropriate

tailoring of care to individual patients. The observed frequency of guideline adherence prior to

initiating the CHAIN Cohort study was comparable or better than other studies in high- and

low-income settings.[12,18–23,27] However, several areas for improvement were identified.

Three areas of suboptimal adherence, or poor record keeping, were anemia diagnosis, HIV

and malaria testing, and hypoxemia assessment and treatment. Medical note reviews cannot

discriminate inadequate record keeping from poor practice. However, this exercise does high-

light the importance of adequate record-keeping, which can be enhanced by pre-formatted

structured medical notes, and can lead to improvements in clinical care.[18,34,35]

Antibiotics were almost universally prescribed when indicated and adherence to recom-

mended regimens was comparable or higher than other studies.[12,20–27] Similar to other

published data, antibiotics were also frequently prescribed to children without an indication.

[24–26] A high proportion of antibiotic prescriptions for children with diarrhea and malaria

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could be explained by differential diagnoses requiring empiric antibiotic treatment. This find-

ing echoes a recent large observational study in Kenya that found 84% of children with diar-

rhea and dehydration were diagnosed with at least one additional condition.[17] This suggests

that helping clinicians confidently exclude these differential diagnoses could considerably

improve antibiotic stewardship. The CHAIN Network now provides malaria and HIV screen-

ing to all enrolled children, chest radiographs to children when indicated, and microbiological

diagnostic support which may increase the specificity of clinical diagnoses. However, a recent

Cochrane review demonstrated that introduction of diagnostic tests, such as malaria rapid

diagnostics, can have unpredictable influences on antimicrobial utilization patterns.[26]

Malnutrition screening protocols varied across sites, with several hospitals neither using

MUAC nor screening all pediatric admissions. Some key informants expressed concern that

expanding indications for specialist nutrition services would increase strain on already over-

burdened clinical staff. Concerns were raised by some interviewees about introducing MUAC,

including suitability for inpatient settings, especially at national or regional referral hospitals.

Children with SAM and low MUAC are typically a higher risk group than those identified by

WHZ alone;[36–38] the CHAIN Network will work with all sites to implement routine screen-

ing using both anthropometrics.

Site leaders related many aspects of inconsistent guideline adherence to low doctor- and

nurse-to-patient ratios, frequent rotation of trainees, and difficulty providing adequate super-

vision of junior clinicians. Insufficient nursing personnel was universally noted by site leader-

ship to be problematic, this was consistent even across a wide range of nurse-to-patient ratios.

The WHO offers advice on numbers of skilled health personnel needed at the population level,

[39] but we are unaware of staffing recommendations at the facility level. Previous studies, typ-

ically in high-income countries, have used staff-per-bed ratios to represent human resource

capacity, assuming that hospital beds are proportional to patient volumes.[40–42] Facilities in

resource-limited settings often experience patient volumes beyond their bed capacity, and con-

sequently double or triple patients-per-bed, add beds outside designated ward areas, or use

floor space to accommodate more patients. In these facilities, staff-per-1000 admissions may

be a better metric for patient volume. The Access, Bottlenecks, Costs and Equity (ABCE) proj-

ect, found that 625 hospitals in Kenya, Uganda, and Zambia had a mean of 7.2, 6.1, and 3.8

doctors-per-100 beds, respectively. They also identified a mean of 49.3, 46.1, and 22.0 nurse-

per-100 beds. The CHAIN sites had similar doctor-, but lower nurse-to-bed ratios, which may

reflect their public ownership, whereas ABCE included private hospitals.[43] Our assessment,

and the ABCE analysis, noted substantial variation in human resources between sites. Quality

assessment and improvement initiatives would benefit from institutional-level staffing bench-

marks that represent efficiency and quality of care.

Our evaluation had several limitations. First, sites were included because they are CHAIN

Network members and were not selected as a representative sample of low- and middle-

income country hospitals. The notes review was a convenience sample and was not powered to

make definitive statements about clinical practices at each site, test association between facility

level factors and guideline adherence, or assess the impact of non-adherence on mortality.

Additionally, a clinical notes review does not capture many important aspects of care, such as

the quality of health education provided to caretakers, and cannot differentiate weak docu-

mentation from poor practice. Next, we assessed inappropriate use of intravenous fluid

boluses, blood transfusions, and antibiotics in the context of diarrhea, because these treatments

may cause adverse effects, especially if used inappropriately. However, we did not assess the

role of non-adherent “overuse” of diagnostics or therapeutics in consuming, and thereby

diverting, limited resources from utilization for appropriate care. Finally, assessment of stock-

outs may have been subject to recall bias, social desirability bias may have influenced aspects

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PLOS ONE | https://doi.org/10.1371/journal.pone.0212395 March 25, 2019 13 / 17

of the qualitative data, and inter-rater reliability of clinical notes abstraction were not assessed.

Despite these limitations, this study utilized a multiple assessment methodology which builds

on previous quality assessment work and provides a template for a systematic assessment of

pediatric inpatient capacity and care across diverse settings in multiple countries.

Conclusion

The CHAIN Network sites had the infrastructure and equipment necessary to implement a

standard of care that met or exceeded WHO recommendations. Despite this capacity, adher-

ence to standardized care guidelines among children treated prior to CHAIN research activi-

ties was inconsistent. Some discrepancies might reflect appropriate tailoring of care to

individual patients. Stretched human resources and stockouts of medicines, nutritional thera-

peutics, and laboratory supplies were the most commonly reported barriers to guideline imple-

mentation. Clinical staffing benchmarks at the facility-level would greatly enhance quality

assessment and improvement efforts. Finally, health worker time requirements should be

assessed when testing implementation of novel inpatient diagnostics and treatments, as it may

be a critical determinant of effectiveness outside of clinical trial conditions.

Supporting information

S1 File. Details of data collection, comparable adherence estimates, high dependency

scores and ward specific equipment scores.

(DOCX)

S1 Appendix. List of CHAIN network authors.

(DOCX)

Author Contributions

Conceptualization: Kirkby D. Tickell, Priya Sukhtankar, James A. Berkley, Judd L. Walson,

Donna M. Denno.

Data curation: Kirkby D. Tickell, Dorothy I. Mangale, Stephanie N. Tornberg-Belanger,

Celine Bourdon, Johnstone Thitiri, Molline Timbwa, Abu S. M. S. B. Shahid.

Formal analysis: Kirkby D. Tickell, Dorothy I. Mangale, Stephanie N. Tornberg-Belanger.

Funding acquisition: James A. Berkley, Judd L. Walson.

Investigation: Kirkby D. Tickell, Johnstone Thitiri, Molline Timbwa, Jenala Njirammadzi,

Wieger Voskuijl, Mohammod J. Chisti, Tahmeed Ahmed, Abu S. M. S. B. Shahid, Abdou-

laye H. Diallo, Issaka Ouedrago, Al Fazal Khan, Ali F. Saleem, Fehmina Arif, Zaubina Kazi,

Ezekiel Mupere, John Mukisa, Priya Sukhtankar, James A. Berkley, Judd L. Walson, Donna

M. Denno.

Methodology: Kirkby D. Tickell, Dorothy I. Mangale, Priya Sukhtankar, James A. Berkley,

Judd L. Walson, Donna M. Denno.

Project administration: Kirkby D. Tickell, Dorothy I. Mangale, Abu S. M. S. B. Shahid,

Donna M. Denno.

Resources: Abu S. M. S. B. Shahid.

Supervision: Kirkby D. Tickell, Donna M. Denno.

Validation: Abu S. M. S. B. Shahid.

Barriers to implementing pediatric inpatient care guidelines

PLOS ONE | https://doi.org/10.1371/journal.pone.0212395 March 25, 2019 14 / 17

Visualization: Kirkby D. Tickell, Dorothy I. Mangale.

Writing – original draft: Kirkby D. Tickell.

Writing – review & editing: Kirkby D. Tickell, Dorothy I. Mangale, Stephanie N. Tornberg-

Belanger, Celine Bourdon, Johnstone Thitiri, Molline Timbwa, Jenala Njirammadzi, Wie-

ger Voskuijl, Mohammod J. Chisti, Tahmeed Ahmed, Abu S. M. S. B. Shahid, Abdoulaye

H. Diallo, Al Fazal Khan, Ali F. Saleem, Zaubina Kazi, Ezekiel Mupere, John Mukisa, Priya

Sukhtankar, James A. Berkley, Judd L. Walson, Donna M. Denno.

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